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Klebsiella and Providencia Emerge As Lone Survivors Following Long-Term Starvation of Oral Microbiota

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Klebsiella and Providencia Emerge As Lone Survivors Following Long-Term Starvation of Oral Microbiota Klebsiella and Providencia emerge as lone survivors following long-term starvation of oral microbiota Jonathon L. Bakera, Erik L. Hendricksonb, Xiaoyu Tanga, Renate Luxc, Xuesong Hed, Anna Edlunda, Jeffrey S. McLeanb, and Wenyuan Shid,1 aGenomic Medicine Group, J. Craig Venter Institute, La Jolla, CA 92037; bDepartment of Periodontics, School of Dentistry, University of Washington, Seattle, WA 98195; cDepartment of Oral Biology, School of Dentistry, University of California, Los Angeles, CA 90095; and dDepartment of Microbiology, The Forsyth Institute, Cambridge, MA 02142 Edited by Jeff F. Miller, University of California, Los Angeles, CA, and approved March 20, 2019 (received for review December 3, 2018) It is well-understood that many bacteria have evolved to survive acids as a source of carbon and energy (4). Therefore, it was catastrophic events using a variety of mechanisms, which include likely that in a complex multispecies community, a succession of expression of stress-response genes, quiescence, necrotrophy, and species and strains would increase and decrease in relative metabolic advantages obtained through mutation. However, the abundance throughout the course of the experiment, based on dynamics of individuals leveraging these abilities to gain a compet- which species were most fit in the changing environment. itive advantage in an ecologically complex setting remain unstudied. To our knowledge, there have been no previous reports on the In this study, we observed the saliva microbiome throughout the interplay of a complex community of human-associated bacteria ecological perturbation of long-term starvation, allowing only the subjected to long-term starvation. To begin to address this knowl- species best equipped to access and use the limited resources to edge gap, the present study monitored a saliva-derived complex survive. During the first several days, the community underwent a oral microbiota during starvation in saline solution and saliva for death phase that resulted in a ∼50–100-fold reduction in the num- 100 d. The bacterial community residing in the human oral cavity is ber of viable cells. Interestingly, after this death phase, only three a particularly unique microbiota that undergoes cyclical expansions species, Klebsiella pneumoniae, Klebsiella oxytoca, and Providen- and contractions of microbial diversity as a result of both host food cia alcalifaciens, all members of the family Enterobacteriaceae, ingestion intervals and hygienic practices, such as brushing and use appeared to be transcriptionally active and recoverable. Klebsiella of mouthwash. These perturbations respectively result in cycles of MICROBIOLOGY are significant human pathogens, frequently resistant to multiple relative feast or famine and regular killing or removal of large antibiotics, and recently, ectopic colonization of the gut by oral swaths of the microbial population, after which ecological succes- Klebsiella was documented to induce dysbiosis and inflammation. sion begins anew (10). Dental caries and periodontitis represent MetaOmics analyses provided several leads for further investiga- two extremely prevalent and costly diseases that are now rec- tion regarding the ecological success of the Enterobacteriaceae. ognized as the result of localized ecological catastrophes of the The isolates accumulated single nucleotide polymorphisms in known growth advantage in stationary phase alleles and produced natural Significance products closely resembling antimicrobial cyclic depsipeptides. The results presented in this study suggest that pathogenic Enterobacter- This study illustrates the dynamics of the oral microbiome iaceae persist much longer than their more benign neighbors in the during long-term starvation. After an initial ecological collapse, salivary microbiome when faced with starvation. This is particularly only three species were recoverable and displayed significant significant, given that hospital surfaces contaminated with oral flu- transcriptional activity: Klebsiella pneumoniae, Klebsiella oxy- ids, especially sinks and drains, are well-established sources of out- toca, and Providencia alcalifaciens. Klebsiella spp. are signifi- breaks of drug-resistant Enterobacteriaceae. cant human pathogens and are frequently resistant to multiple classes of antibiotics. In addition to its status as a clinical oral microbiome | microbial ecology | Klebsiella scourge in its own right, K. pneumoniae has emerged as a chief facilitator in the transfer of drug resistance genes from the any bacteria are well-equipped to deal with exposure to environment to pathogens. Hospital surfaces contaminated Madverse environmental events such as starvation, oxidative with oral fluids are well-documented sources of outbreaks of stress, and antimicrobials, as well as fluctuations in temperature, drug-resistant Enterobacteriaceae; therefore, the ability of pH, and osmolality. Diverse strategies for coping with these Klebsiella to outcompete its neighbors during starvation and stresses have evolved, including expression of stress response survive long-term in saliva is particularly noteworthy. genes (1), quiescence (2), necrotrophy (3), and growth advan- tages gained through mutation (4). Although these systems are Author contributions: J.L.B., X.H., J.S.M., and W.S. designed research; J.L.B., E.L.H., X.T., A.E., and J.S.M. performed research; J.L.B., E.L.H., R.L., X.H., A.E., J.S.M., and W.S. analyzed increasingly understood, little is known regarding the dynamics data; and J.L.B. wrote the paper. of individual species leveraging these abilities to gain a com- Conflict of interest statement: J.L.B. is a part-time consultant for uBiome, Inc. W.S. is a petitive advantage in an ecologically complex setting. In the case part-time chief science officer of C3J Therapeutics, Inc., which has licensed technologies of long-term starvation, the bulk of research on bacterial dy- from the University of California Regents that could be indirectly related to this namics and survival mechanisms has been performed using research project. monospecies cultures of Escherichia coli (4–9). In E. coli, pop- This article is a PNAS Direct Submission. ulations exhibited a death phase at ∼3 d of starvation, resulting This open access article is distributed under Creative Commons Attribution-NonCommercial- in a loss of >99% of the population (4). This death phase was NoDerivatives License 4.0 (CC BY-NC-ND). followed by a long-term stationary phase, in which viable cell Data deposition: The raw sequencing files used in the genomic, metagenomic, and tran- scriptomic analyses in this study have been deposited in the Sequence Read Archive, https:// counts plateau virtually indefinitely (i.e., for years) (4). During www.ncbi.nlm.nih.gov/sra [accession nos. PRJNA525688 (genomes) and PRJNA525517 the long-term stationary phase, various subpopulations carrying (metagenomes/transcriptomes)]. advantageous mutations (growth advantage in stationary phase 1To whom correspondence should be addressed. Email: [email protected]. [GASP] mutants) arose and came to dominate the culture, dis- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. placing their less-fit siblings (4). These mutations frequently 1073/pnas.1820594116/-/DCSupplemental. resulted in increased ability to catabolize one or more amino Published online April 11, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1820594116 PNAS | April 23, 2019 | vol. 116 | no. 17 | 8499–8504 Downloaded by guest on September 26, 2021 oral microbiome (11–14). One of the major impediments to the study AB9 of complex, human-associated microbial communities is the difficulty 10 PBS:saliva 7 *** cultivating such diverse ecologies in a well-controlled laboratory 108 PBS setting. The oral microbiota was chosen as a model system for this 107 6 pilot study because of the existence of a well-established in vitro 106 CFU/ml 5 culture system using media that allows for the growth of a diversity of 105 Shannon Index 4 species approaching that of an in vivo human mouth (15). 104 PBS:saliva PBS 050100 Time (days) 84 Results CDPBS:saliva 72 7 PC2 (23.8%) PBS 59 Long-Term Starvation of a Complex Oral Community Results in a **** 45 32 Death Phase, Followed by a Long-Term Stationary Phase. The start- 6 20 12 ing community in this study was derived from a previous study 4 5 2 that optimized media (SHI media) and growth conditions to Days of Starvation 1 stably maintain the highest diversity of oral bacteria achievable Shannon Index 0 4 PC1 (51.4%) 0 in vitro to date (15). The community was generated from the 1 2 4 12 20 32 45 59 72 84 PC3 (3.7%) pooled saliva of six healthy adults, had a microbial diversity Days of Starvation PBS:saliva PBS:saliva outgrowth approaching that of human oral cavity, and responded to a E starving community in fresh media carbohydrate pulse in a manner similar to in vivo dental plaque Days of Starvation 0 1 4 12203245597284 0 4 12 32 59 84 (15). After overnight batch growth in SHI media, the community Proteus Enterobacteriacae; other was harvested and subsequently starved in aliquots of either PBS Kluyvera or a 1:1 mixture of PBS and cell-free saliva. Reminiscent of Klebsiella Enterobacter monospecies cultures of E. coli (4), the communities (both in Neisseria Klebsiella Other PBS and PBS:saliva) first experienced a death phase with a rapid Fusobacterium decrease in colony-forming units per milliliter over time, fol- Veillonella Peptostreptococcus lowed by a stabilization, a long-term stationary phase
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